Multicenter Study

. 2023 Jan;43(1):47-58.

doi: 10.1007/s00296-022-05229-7. Epub 2022 Oct 22.

COVID-19 severity and vaccine breakthrough infections in idiopathic inflammatory myopathies, other systemic autoimmune and inflammatory diseases, and healthy controls: a multicenter cross-sectional study from the COVID-19 Vaccination in Autoimmune Diseases (COVAD) survey

Leonardo Santos Hoff¹, Naveen Ravichandran², Samuel Katsuyuki Shinjo³, Jessica Day^{4

5

6}, Parikshit Sen⁷, Jucier Gonçalves Junior³, James B Lilleker^{8

9}, Mrudula Joshi¹⁰, Vishwesh Agarwal¹¹, Sinan Kardes¹², Minchul Kim¹³, Marcin Milchert¹⁴, Ashima Makol¹⁵, Tamer Gheita¹⁶, Babur Salim¹⁷, Tsvetelina Velikova¹⁸, Abraham Edgar Gracia-Ramos¹⁹, Ioannis Parodis^{20

21}, Albert Selva O'Callaghan²², Elena Nikiphorou^{23

24}, Ai Lyn Tan^{25

26}, Tulika Chatterjee¹³, Lorenzo Cavagna^{27

28}, Miguel A Saavedra²⁹, Nelly Ziade^{30

31}, Johannes Knitza³², Masataka Kuwana³³, Arvind Nune³⁴, Oliver Distler³⁵, Döndü Üsküdar Cansu³⁶, Lisa Traboco³⁷, Suryo Angorro Kusumo Wibowo³⁸, Erick Adrian Zamora Tehozol³⁹, Jorge Rojas Serrano⁴⁰, Ignacio García-De La Torre⁴¹, Chris Wincup^{42

43}, John D Pauling^{44

45}, Hector Chinoy^{8

46

47}, Vikas Agarwal², Rohit Aggarwal^#⁴⁸, Latika Gupta^#^{49

50

51

52}; COVAD Study Group

Affiliations

¹ School of Medicine, Universidade Potiguar (UnP), Natal, Brazil.
² Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India.
³ Division of Rheumatology, Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.
⁴ Department of Rheumatology, Royal Melbourne Hospital, Parkville, VIC, 3050, Australia.
⁵ Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia.
⁶ Department of Medical Biology, University of Melbourne, Parkville, VIC, 3052, Australia.
⁷ Maulana Azad Medical College, 2-Bahadurshah Zafar Marg, New Delhi, Delhi, 110002, India.
⁸ Centre for Musculoskeletal Research, Division of Musculoskeletal and Dermatological Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, The University of Manchester, Manchester, UK.
⁹ Neurology, Manchester Centre for Clinical Neurosciences, Northern Care Alliance NHS Foundation Trust, Salford, UK.
¹⁰ Byramjee Jeejeebhoy Government Medical College and Sassoon General Hospitals, Pune, India.
¹¹ Mahatma Gandhi Mission Medical College, Navi Mumbai, Maharashtra, India.
¹² Department of Medical Ecology and Hydroclimatology, Istanbul Faculty of Medicine, Istanbul University, Capa-Fatih, 34093, Istanbul, Turkey.
¹³ Center for Outcomes Research, Department of Internal Medicine, University of Illinois College of Medicine, Peoria, IL, USA.
¹⁴ Department of Internal Medicine, Rheumatology, Geriatrics and Clinical Immunology, Pomeranian Medical University in Szczecin, ul Unii Lubelskiej 1, 71-252, Szczecin, Poland.
¹⁵ Division of Rheumatology, Mayo Clinic, Rochester, MN, USA.
¹⁶ Rheumatology Department, Kasr Al Ainy School of Medicine, Cairo University, Cairo, Egypt.
¹⁷ Rheumatology Department, Fauji Foundation Hospital, Rawalpindi, Pakistan.
¹⁸ Department of Clinical Immunology, Medical Faculty, University Hospital "Lozenetz", Sofia University St. Kliment Ohridski, 1 Kozyak Str., 1407, Sofia, Bulgaria.
¹⁹ Department of Internal Medicine, General Hospital, National Medical Center, La Raza", Instituto Mexicano del Seguro Social, Av. Jacaranda S/N, Col. La Raza, Del. Azcapotzalco, 02990, Mexico City, Mexico.
²⁰ Division of Rheumatology, Department of Medicine Solna, Karolinska Institutet and Karolinska University Hospital, Stockholm, Sweden.
²¹ Department of Rheumatology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.
²² Internal Medicine Department, Vall D'hebron General Hospital, Universitat Autonoma de Barcelona, 08035, Barcelona, Spain.
²³ Centre for Rheumatic Diseases, King's College London, London, UK.
²⁴ Rheumatology Department, King's College Hospital, London, UK.
²⁵ NIHR Leeds Biomedical Research Centre, Leeds Teaching Hospitals Trust, Leeds, UK.
²⁶ Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, Leeds, UK.
²⁷ Department of Rheumatology, Fondazione I.R.C.C.S. Policlinico San Matteo, Pavia, Italy.
²⁸ Rheumatology Unit, Dipartimento di Medicine Interna e Terapia Medica, Università degli studi di Pavia, Lombardy, Pavia, Italy.
²⁹ Departamento de Reumatología Hospital de Especialidades Dr. Antonio Fraga Mouret, Centro Médico Nacional La Raza, IMSS, Mexico City, Mexico.
³⁰ Rheumatology Department, Saint-Joseph University, Beirut, Lebanon.
³¹ Rheumatology Department, Hotel-Dieu de France Hospital, Beirut, Lebanon.
³² Medizinische Klinik 3-Rheumatologie und Immunologie, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Ulmenweg 18, 91054, Erlangen, Germany.
³³ Department of Allergy and Rheumatology, Nippon Medical School Graduate School of Medicine, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan.
³⁴ Southport and Ormskirk Hospitals NHS Trust, Southport, PR8 6PN, UK.
³⁵ Department of Rheumatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
³⁶ Division of Rheumatology, Department of Internal Medicine, Eskişehir Osmangazi University, 26480, Eskişehir, Turkey.
³⁷ Philippine Rheumatology Association, St Luke's Medical Center-Global City, Taguig, Philippines.
³⁸ Rheumatology Division, Department of Internal Medicine, Fakultas Kedokteran, Universitas Indonesia, Jakarta, Indonesia.
³⁹ Rheumatology, Medical Care and Research, Centro Medico Pensiones Hospital, Instituto Mexicano del Seguro Social Delegación Yucatán, Yucatán, Mexico.
⁴⁰ Rheumatologist and Clinical Investigator, Interstitial Lung Disease and Rheumatology Unit, Instituto Nacional de Enfermedades Respiratorias, Mexico City, Mexico.
⁴¹ Departamento de Inmunología y Reumatología, Hospital General de Occidente and University of Guadalajara, Guadalajara, Jalisco, Mexico.
⁴² Department of Rheumatology, Division of Medicine, Rayne Institute, University College London, London, UK.
⁴³ Centre for Adolescent Rheumatology Versus Arthritis at UCL, UCLH, GOSH, London, UK.
⁴⁴ Bristol Medical School Translational Health Sciences, University of Bristol, Bristol, UK.
⁴⁵ Department of Rheumatology, North Bristol NHS Trust, Bristol, UK.
⁴⁶ National Institute for Health Research Manchester Biomedical Research Centre, Manchester University NHS Foundation Trust, The University of Manchester, Manchester, UK.
⁴⁷ Department of Rheumatology, Salford Royal Hospital, Northern Care Alliance NHS Foundation Trust, Salford, UK.
⁴⁸ Division of Rheumatology and Clinical Immunology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
⁴⁹ Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India. drlatikagupta@gmail.com.
⁵⁰ Centre for Musculoskeletal Research, Division of Musculoskeletal and Dermatological Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, The University of Manchester, Manchester, UK. drlatikagupta@gmail.com.
⁵¹ Department of Rheumatology, Royal Wolverhampton Hospitals NHS Trust, Wolverhampton, WV10 0QP, UK. drlatikagupta@gmail.com.
⁵² City Hospital, Sandwell and West Birmingham Hospitals NHS Trust, Birmingham, UK. drlatikagupta@gmail.com.

^# Contributed equally.

PMID: 36271958
PMCID: PMC9589602
DOI: 10.1007/s00296-022-05229-7

Multicenter Study

COVID-19 severity and vaccine breakthrough infections in idiopathic inflammatory myopathies, other systemic autoimmune and inflammatory diseases, and healthy controls: a multicenter cross-sectional study from the COVID-19 Vaccination in Autoimmune Diseases (COVAD) survey

Leonardo Santos Hoff et al. Rheumatol Int. 2023 Jan.

. 2023 Jan;43(1):47-58.

doi: 10.1007/s00296-022-05229-7. Epub 2022 Oct 22.

Authors

Affiliations

¹ School of Medicine, Universidade Potiguar (UnP), Natal, Brazil.
² Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India.
³ Division of Rheumatology, Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.
⁴ Department of Rheumatology, Royal Melbourne Hospital, Parkville, VIC, 3050, Australia.
⁵ Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia.
⁶ Department of Medical Biology, University of Melbourne, Parkville, VIC, 3052, Australia.
⁷ Maulana Azad Medical College, 2-Bahadurshah Zafar Marg, New Delhi, Delhi, 110002, India.
⁸ Centre for Musculoskeletal Research, Division of Musculoskeletal and Dermatological Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, The University of Manchester, Manchester, UK.
⁹ Neurology, Manchester Centre for Clinical Neurosciences, Northern Care Alliance NHS Foundation Trust, Salford, UK.
¹⁰ Byramjee Jeejeebhoy Government Medical College and Sassoon General Hospitals, Pune, India.
¹¹ Mahatma Gandhi Mission Medical College, Navi Mumbai, Maharashtra, India.
¹² Department of Medical Ecology and Hydroclimatology, Istanbul Faculty of Medicine, Istanbul University, Capa-Fatih, 34093, Istanbul, Turkey.
¹³ Center for Outcomes Research, Department of Internal Medicine, University of Illinois College of Medicine, Peoria, IL, USA.
¹⁴ Department of Internal Medicine, Rheumatology, Geriatrics and Clinical Immunology, Pomeranian Medical University in Szczecin, ul Unii Lubelskiej 1, 71-252, Szczecin, Poland.
¹⁵ Division of Rheumatology, Mayo Clinic, Rochester, MN, USA.
¹⁶ Rheumatology Department, Kasr Al Ainy School of Medicine, Cairo University, Cairo, Egypt.
¹⁷ Rheumatology Department, Fauji Foundation Hospital, Rawalpindi, Pakistan.
¹⁸ Department of Clinical Immunology, Medical Faculty, University Hospital "Lozenetz", Sofia University St. Kliment Ohridski, 1 Kozyak Str., 1407, Sofia, Bulgaria.
¹⁹ Department of Internal Medicine, General Hospital, National Medical Center, La Raza", Instituto Mexicano del Seguro Social, Av. Jacaranda S/N, Col. La Raza, Del. Azcapotzalco, 02990, Mexico City, Mexico.
²⁰ Division of Rheumatology, Department of Medicine Solna, Karolinska Institutet and Karolinska University Hospital, Stockholm, Sweden.
²¹ Department of Rheumatology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.
²² Internal Medicine Department, Vall D'hebron General Hospital, Universitat Autonoma de Barcelona, 08035, Barcelona, Spain.
²³ Centre for Rheumatic Diseases, King's College London, London, UK.
²⁴ Rheumatology Department, King's College Hospital, London, UK.
²⁵ NIHR Leeds Biomedical Research Centre, Leeds Teaching Hospitals Trust, Leeds, UK.
²⁶ Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, Leeds, UK.
²⁷ Department of Rheumatology, Fondazione I.R.C.C.S. Policlinico San Matteo, Pavia, Italy.
²⁸ Rheumatology Unit, Dipartimento di Medicine Interna e Terapia Medica, Università degli studi di Pavia, Lombardy, Pavia, Italy.
²⁹ Departamento de Reumatología Hospital de Especialidades Dr. Antonio Fraga Mouret, Centro Médico Nacional La Raza, IMSS, Mexico City, Mexico.
³⁰ Rheumatology Department, Saint-Joseph University, Beirut, Lebanon.
³¹ Rheumatology Department, Hotel-Dieu de France Hospital, Beirut, Lebanon.
³² Medizinische Klinik 3-Rheumatologie und Immunologie, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Ulmenweg 18, 91054, Erlangen, Germany.
³³ Department of Allergy and Rheumatology, Nippon Medical School Graduate School of Medicine, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan.
³⁴ Southport and Ormskirk Hospitals NHS Trust, Southport, PR8 6PN, UK.
³⁵ Department of Rheumatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
³⁶ Division of Rheumatology, Department of Internal Medicine, Eskişehir Osmangazi University, 26480, Eskişehir, Turkey.
³⁷ Philippine Rheumatology Association, St Luke's Medical Center-Global City, Taguig, Philippines.
³⁸ Rheumatology Division, Department of Internal Medicine, Fakultas Kedokteran, Universitas Indonesia, Jakarta, Indonesia.
³⁹ Rheumatology, Medical Care and Research, Centro Medico Pensiones Hospital, Instituto Mexicano del Seguro Social Delegación Yucatán, Yucatán, Mexico.
⁴⁰ Rheumatologist and Clinical Investigator, Interstitial Lung Disease and Rheumatology Unit, Instituto Nacional de Enfermedades Respiratorias, Mexico City, Mexico.
⁴¹ Departamento de Inmunología y Reumatología, Hospital General de Occidente and University of Guadalajara, Guadalajara, Jalisco, Mexico.
⁴² Department of Rheumatology, Division of Medicine, Rayne Institute, University College London, London, UK.
⁴³ Centre for Adolescent Rheumatology Versus Arthritis at UCL, UCLH, GOSH, London, UK.
⁴⁴ Bristol Medical School Translational Health Sciences, University of Bristol, Bristol, UK.
⁴⁵ Department of Rheumatology, North Bristol NHS Trust, Bristol, UK.
⁴⁶ National Institute for Health Research Manchester Biomedical Research Centre, Manchester University NHS Foundation Trust, The University of Manchester, Manchester, UK.
⁴⁷ Department of Rheumatology, Salford Royal Hospital, Northern Care Alliance NHS Foundation Trust, Salford, UK.
⁴⁸ Division of Rheumatology and Clinical Immunology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
⁴⁹ Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India. drlatikagupta@gmail.com.
⁵⁰ Centre for Musculoskeletal Research, Division of Musculoskeletal and Dermatological Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, The University of Manchester, Manchester, UK. drlatikagupta@gmail.com.
⁵¹ Department of Rheumatology, Royal Wolverhampton Hospitals NHS Trust, Wolverhampton, WV10 0QP, UK. drlatikagupta@gmail.com.
⁵² City Hospital, Sandwell and West Birmingham Hospitals NHS Trust, Birmingham, UK. drlatikagupta@gmail.com.

^# Contributed equally.

PMID: 36271958
PMCID: PMC9589602
DOI: 10.1007/s00296-022-05229-7

Abstract

Objectives: We aimed to compare the spectrum and severity of COVID-19 and vaccine breakthrough infections (BIs) among patients with IIMs, other systemic autoimmune and inflammatory diseases (SAIDs), and healthy controls (HCs).

Methods: This is a cross-sectional study with data from the COVAD study, a self-reported online global survey that collected demographics, COVID-19 history, and vaccination details from April to September 2021. Adult patients with at least one COVID-19 vaccine dose were included. BIs were defined as infections occurring > 2 weeks after any dose of vaccine. Characteristics associated with BI were analyzed with a multivariate regression analysis.

Results: Among 10,900 respondents [42 (30-55) years, 74%-females, 45%-Caucasians] HCs were (47%), SAIDs (42%) and IIMs (11%). Patients with IIMs reported fewer COVID-19 cases before vaccination (6.2%-IIM vs 10.5%-SAIDs vs 14.6%-HC; OR = 0.6, 95% CI 0.4-0.8, and OR = 0.3, 95% CI 0.2-0.5, respectively). BIs were uncommon (1.4%-IIM; 1.9%-SAIDs; 3.2%-HC) and occurred in 17 IIM patients, 13 of whom were on immunosuppressants, and 3(18%) required hospitalization. All-cause hospitalization was higher in patients with IIM compared to HCs [23 (30%) vs 59 (8%), OR = 2.5, 95% CI 1.2-5.1 before vaccination, and 3 (18%) vs 9 (5%), OR = 2.6, 95% CI 1.3-5.3 in BI]. In a multivariate regression analysis, age 30-60 years was associated with a lower odds of BI (OR = 0.7, 95% CI 0.5-1.0), while the use of immunosuppressants had a higher odds of BI (OR = 1.6, 95% CI 1.1-2.7).

Conclusions: Patients with IIMs reported fewer COVID-19 cases than HCs and other SAIDs, but had higher odds of all-cause hospitalization from COVID-19 than HCs. BIs were associated with the use of immunosuppressants and were uncommon in IIMs.

Keywords: Autoimmune diseases; Breakthrough infection; COVID-19; Idiopathic inflammatory myopathies; SARS-CoV-2 vaccination.

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Conflict of interest statement

ALT has received honoraria for advisory boards and speaking for Abbvie, Gilead, Janssen, Lilly, Novartis, Pfizer, UCB. CW has received travel support from Abbvie, unrelated to this manuscript. EN has received speaker honoraria/participated in advisory boards for Celltrion, Pfizer, Sanofi, Gilead, Galapagos, AbbVie, Lilly and holds research grants from Pfizer and Lilly. HC has received grant support from Eli Lilly and UCB; consulting fees from Novartis, Eli Lilly, Orphazyme, Astra Zeneca; speaker for UCB, Biogen. HC is supported by the National Institution for Health Research Manchester Biomedical Research Centre Funding Scheme. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health. IP has received research funding and/or honoraria from Amgen, AstraZeneca, Aurinia Pharmaceuticals, Elli Lilly and Company, Gilead Sciences, GlaxoSmithKline, Janssen Pharmaceuticals, Novartis and F. Hoffmann-La Roche AG. JD has received research funding from CSL Limited. JBL has received speaker honoraria/participated in advisory boards for Sanofi Genzyme, Roche, and Biogen. None is related to this manuscript. JP has received consulting fees, speaking fees, and/or honoraria from Actelion, Sojournix Pharma, and Boehringer Ingelheim. None is related to this manuscript. NZ has received speaker fees, advisory board fees and research grants from Pfizer, Roche, Abbvie, Eli Lilly, NewBridge, Sanofi-Aventis, Boehringer Ingelheim, Janssen, Pierre Fabre; none is related to this manuscript. OD has/had consultancy relationship with and/or has received research funding from or has served as a speaker for the following companies in the area of potential treatments for systemic sclerosis and its complications in the last three years: Abbvie, Acceleron, Alcimed, Amgen, AnaMar, Arxx, Baecon, Blade, Bayer, Boehringer Ingelheim, ChemomAb, Corbus, CSL Behring, Galapagos, Glenmark, GSK, Horizon (Curzion), Inventiva, iQvia, Kymera, Lupin, Medac, Medscape, Mitsubishi Tanabe, Novartis, Roche, Roivant, Sanofi, Serodapharm, Topadur and UCB. Patent issued “mir-29 for the treatment of systemic sclerosis” (US8247389, EP2331143). RA has/had a consultancy relationship with and/or has received research funding from the following companies-Bristol Myers-Squibb, Pfizer, Genentech, Octapharma, CSL Behring, Mallinckrodt, AstraZeneca, Corbus, Kezar, and Abbvie, Janssen, Alexion, Argenx, Q32, EMD-Serono, Boehringer Ingelheim, Roivant. Rest of the authors have no conflict of interest relevant to this manuscript.

Figures

**Fig. 1**
Flow diagram of study participants

See this image and copyright information in PMC

References

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COVID-19 severity and vaccine breakthrough infections in idiopathic inflammatory myopathies, other systemic autoimmune and inflammatory diseases, and healthy controls: a multicenter cross-sectional study from the COVID-19 Vaccination in Autoimmune Diseases (COVAD) survey

Affiliations

COVID-19 severity and vaccine breakthrough infections in idiopathic inflammatory myopathies, other systemic autoimmune and inflammatory diseases, and healthy controls: a multicenter cross-sectional study from the COVID-19 Vaccination in Autoimmune Diseases (COVAD) survey

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Substances

Supplementary concepts

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Miscellaneous